Extreme Inbreeding Research Articles

Extreme nearly neutral evolution in mitochondrial genomes of laboratory mouse strains

Relaxation of the selective constraint during the domestication process is known. In this study, we report unexpected closeness to neutral evolution of mitochondrial genomes of laboratory mouse strains: estimated non-synonymous/synonymous rate ratio being very close to 1 (ω^=1.32). Probably it is due to the extreme inbreeding extending over 100years as well as to their recent origin (middle of the last millennium). There is no rate difference observed among three codon positions as well as ribosomal RNA and control regions. However, the amino acid substitutions occurred not randomly, and substitutions were more frequent between physico-chemically similar amino acids than between dissimilar ones. Probably this is inevitable consequence caused by the codon table itself, but not by selections. This implies that a large portion of the new mutations are conservative, and most of them are slightly deleterious and not lethal. It seems that, even though the selection pressures do not hold normally, the function of genes may not be impaired in most cases.

Limited male dispersal in a social spider with extreme inbreeding

Cooperatively breeding animals commonly avoid incestuous mating through pre-mating dispersal. However, a few group-living organisms, including the social spiders, have low pre-mating dispersal, intra-colony mating, and inbreeding. This results in limited gene flow among colonies and sub-structured populations. The social spiders also exhibit female-biased sex ratios because survival benefits to large colonies favour high group productivity, which selects against 1 : 1 sex ratios. Although propagule dispersal of mated females may occasionally bring about limited gene flow, little is known about the role of male dispersal. We assessed the extent of male movement between colonies in natural populations both experimentally and by studying colony sex ratios over the mating season. We show that males frequently move to neighbouring colonies, whereas only 4% of incipient nests were visited by dispersing males. Neighbouring colonies are genetically similar and movement within colony clusters does not contribute to gene flow. Post-mating sex ratio bias was high early in the mating season due to protandry, and also in colonies at the end of the season, suggesting that males remain in the colony when mated females have dispersed. Thus, male dispersal is unlikely to facilitate gene flow between different matrilineages. This is consistent with models of non-Fisherian group-level selection for the maintenance of female biased sex ratios, which predict the elimination of male dispersal.

Species cohesion despite extreme inbreeding in a social spider

Colonial social spiders experience extreme inbreeding and highly restricted gene flow between colonies; processes that question the genetic cohesion of geographically separated populations and which could imply multiple origins from predecessors with limited gene flow. We analysed species cohesion and the potential for long-distance dispersal in the social spider Stegodyphus dumicola by studying colony structure in eastern South Africa and the cohesion between this population and Namibian populations previously published. Data from both areas were (re)analysed for historic demographic parameters. Eastern South African S. dumicola were closely related to an east Namibian lineage, showing cohesion of S. dumicola relative to its sister species. Colony structure was similar in both areas with mostly monomorphic colonies, but haplotype diversity was much reduced in eastern South Africa. Here, the population structure indicated recent population expansion. By contrast, Namibia constitutes an old population, possibly the geographic origin of the species. Both the comparison of the eastern South African and Namibian lineages and the distribution within eastern South Africa show the potential for long-distance dispersal in few generations via colony propagation.

Sex differences in the genetic architecture of lifespan in a seed beetle: extreme inbreeding extends male lifespan

BackgroundSex differences in lifespan are ubiquitous throughout the animal kingdom but the causes underlying this phenomenon remain poorly understood. Several explanations based on asymmetrical inheritance patterns (sex chromosomes or mitochondrial DNA) have been proposed, but these ideas have rarely been tested experimentally. Alternatively, sexual dimorphism in lifespan could result from sex-specific selection, caused by fundamental differences in how males and females optimize their fitness by allocating resources into current and future reproduction.ResultsHere we used sex-specific responses to inbreeding to study the genetic architecture of lifespan and mortality rates in Callosobruchus maculatus, a seed beetle that shows sexual dimorphism in lifespan. Two independent assays revealed opposing sex-specific responses to inbreeding. The combined data set showed that inbred males live longer than outbred males, while females show the opposite pattern. Both sexes suffered reduced fitness measured as lifetime reproductive success as a result of inbreeding.ConclusionNo model based on asymmetrical inheritance can explain increased male lifespan in response to inbreeding. Our results are however compatible with models based on sex-specific selection on reproductive strategies. We therefore suggest that sex-specific differences in lifespan in this species primarily result from sexually divergent selection.

Fifteen new microsatellite markers for the reef coral Favia fragum and a new Symbiodinium microsatellite

Sixteen new microsatellite loci were isolated from the Tropical Atlantic coral Favia fragum. One locus amplified with pure zooxanthellae DNA template, revealing a symbiont (Symbiodinium) origin. We genotyped 48 short and 45 tall ecomorphs of F. fragum from the Bocas del Toro region of Panama. For 15 host loci, allelic diversity ranged from three to 23 with an average of 5.75 alleles per locus. Analysis of genotypic data revealed significant heterozygote deficits at all loci and linkage disequilibrium between loci, as did a previous study of the two ecomorphs with allozymes. We found evidence for null alleles at four of the host loci in the form of locus-specific polymerase chain reaction failure; however, extreme inbreeding via self-fertilization is likely to explain the large departures from Hardy-Weinberg equilibrium.

Breeding Designs for Recombinant Inbred Advanced Intercross Lines

Recombinant inbred lines derived from an advanced intercross, in which multiple generations of mating have increased the density of recombination breakpoints, are powerful tools for mapping the loci underlying complex traits. We investigated the effects of intercross breeding designs on the utility of such lines for mapping. The simplest design, random pair mating with each pair contributing exactly two offspring to the next generation, performed as well as the most extreme inbreeding avoidance scheme at expanding the genetic map, increasing fine-mapping resolution, and controlling genetic drift. Circular mating designs offer negligible advantages for controlling drift and exhibit greatly reduced map expansion. Random-mating designs with variance in offspring number are also poor at increasing mapping resolution. Given equal contributions of each parent to the next generation, the constraint of monogamy has no impact on the qualities of the final population of inbred lines. We find that the easiest crosses to perform are well suited to the task of generating populations of highly recombinant inbred lines.

Survival benefits select for group living in a social spider despite reproductive costs

The evolution of cooperation requires benefits of group living to exceed costs. Hence, some components of fitness are expected to increase with increasing group size, whereas others may decrease because of competition among group members. The social spiders provide an excellent system to investigate the costs and benefits of group living: they occur in groups of various sizes and individuals are relatively short-lived, therefore life history traits and Lifetime Reproductive Success (LRS) can be estimated as a function of group size. Sociality in spiders has originated repeatedly in phylogenetically distant families and appears to be accompanied by a transition to a system of continuous intra-colony mating and extreme inbreeding. The benefits of group living in such systems should therefore be substantial. We investigated the effect of group size on fitness components of reproduction and survival in the social spider Stegodyphus dumicola in two populations in Namibia. In both populations, the major benefit of group living was improved survival of colonies and late-instar juveniles with increasing colony size. By contrast, female fecundity, female body size and early juvenile survival decreased with increasing group size. Mean individual fitness, estimated as LRS and calculated from five components of reproduction and survival, was maximized for intermediate- to large-sized colonies. Group living in these spiders thus entails a net reproductive cost, presumably because of an increase in intra-colony competition with group size. This cost is traded off against survival benefits at the colony level, which appear to be the major factor favouring group living. In the field, many colonies occur at smaller size than expected from the fitness curve, suggesting ecological or life history constraints on colony persistence which results in a transient population of relatively small colonies.

Re-thinking the embryo lethal system within the Pinaceae

Outcrossing, wind-pollinated members of the Pinaceae have high self-pollination rates yet produce few selfed seedlings. How are selfs selectively eliminated? Barriers to selfing have long been considered to be (i) avoidance of self-pollen capture, (ii) competition via simple polyembryony, and (iii) lower viability of selfed embryos. Here, reviews — and some revisions — are offered in addition to future research needs. First, avoiding self-pollen capture is largely ineffectual. Second, simple polyembrony is also a weak or nonexistent barrier against selfed embryos. Third, selfed embryos die at all stages, but a stage-specific death peak occurs during early embryogeny in some taxa and this death peak, if prevalent across a wider range of taxa, deserves a closer look. The death peak does not preclude the prevailing genetic model for embryo viability loci, but could indicate that other genetic mechanisms are operative. Molecular dissection shows that zygotic lethals are distributed across different chromosomal segments. To date, these are mostly semi-lethal rather than lethal, and they range from partially dominant to overdominant. A literature survey suggests that only 5 of the 10 genera within the Pinaceae ( Abies , Larix , Picea , Pinus , and Pseudotsuga ) have been well characterized with respect to selfing. Extreme inbreeding depression during embryo development may not be a shared feature among conifers as a group. A critical research question is whether dual death patterns are present in other genera, and if they are, alternative genetic models to account for the death peak. Addressing these questions has broad relevance to conservation, domestication, and management of closed populations, not just conifers or gymnosperms.

Molecular Polymorphism of Strains within Paramecium septaurelia (Ciliophora, Oligohymenophorea)

RAPD-PCR fingerprinting and ARDRA riboprinting revealed polymorphism within P. septaurelia strains from Russia (4 strains from Lower Volga Basin), and one strain from USA, Florida. However, the first method showed the existence of four RAPD genotypes while the second revealed only two groups of strains with different band patterns. All studied strains had a high percentage of surviving hybrid clones in the inter-strain crosses, with little differentiation of strains within species. Intra-species differentiation of strains in RAPD band patterns may be connected with the degree of inbreeding for the studied species. Species of the P. aurelia complex can be arranged according to the degree of inbreeding characteristic for each, which is correlated with the degree of DNA polymorphism revealed by the RAPD method from extreme inbreeders (e.g. P. sexaurelia), moderate inbreeders (e.g. P. triaurelia) to weak inbreeders (e.g. P. pentaurelia). P. septaurelia of the P. aurelia complex should be included in the group of extreme inbreeder.

Polymorphic microsatellite loci in the Coffee Berry Borer, Hypothenemus hampei (Coleoptera, Scolytidae)

AbstractMicrosatellite loci were isolated from the coffee berry borer, Hypothenemus hampei, which is regarded as the major pest in coffee cultures. Seven polymorphic loci were obtained from an enriched genomic library. A low to moderate genetic diversity was observed per locus, with an observed number of alleles ranging from two to five in the 39 unrelated individuals sampled from Ethiopia. A clear deficit of heterozygotes within the population (mean heterozygosities, HO = 0.10/HE = 0.50) and an extreme inbreeding (FIS, 0.70–1.00) were demonstrated. Cross‐species amplifications showed that some of the markers could be useful in two closely related Hypothenemus species.

The consequence of inbreeding for modulating social relationships between competitors

Extreme inbreeding is likely severely to compromise an animal’s ability to discriminate between individuals that are genetically very similar or identical, and thus to assess their familiarity and kinship with conspecifics. We tested whether male laboratory mice of the outbred ICR strain and the inbred BALB/c strain could discriminate between familiar companions and unfamiliar males of their own strain, or between unfamiliar mice from their own or the other strain, by examining both responses to the males’ scents and competitive aggression during direct interactions. Outbred ICR males spent more time investigating odours of unfamiliar males and were more aggressive towards unfamiliar males than towards familiar companions of their own strain. BALB/c males failed to discriminate between familiar and unfamiliar males of their own strain, showing little aggression to both. In contrast, most BALB/c males (17/24) were aggressive towards unfamiliar ICR males and investigated their scent for longer than that from their own strain. The low level of aggression towards unfamiliar own-strain males suggests that the inbred males failed to recognise that unfamiliar individuals were not their familiar cagemates. They were unable to discriminate between different individuals from their own strain using either chemical or other additional cues of individual identity available during direct interaction.

Extraordinary sex ratios and the evolution of male neoteny in sib-mating Ozopemon beetles

The weevil subfamily Scolytinae includes at least seven groups of regularly sib-mating species with extremely female-biased offspring sex ratios. The enigmatic SE-Asian bark beetle genus Ozopemon (25 spp.) belong to the most diversified clade (>1400 spp.) of such ancient inbreeding lineages. While males of all sib-mating scolytines are flightless, and are usually dwarfed versions of their larger sisters, the existence of males in Ozopemon has been a controversial issue. Some strangely modified male beetles, with fully developed aedeagus, strongly flattened pronotum and head, and 10-segmented larviform abdomen, were first described as males of O. brownei, but were later assigned to the Histeridae. With the new evidence provided here, based on DNA sequence data from mitochondrial and nuclear gene partitions, and examination of genitalic characters, we re-assign these males, as well as males for two more species, to Ozopemon. Neoteny evolved close to the origin of sib-mating and possibly haplodiploidy, but the transition to neoteny occurred separately from all other inbreeding dryocoetine and xyleborine beetles. The neotenic development of these males is the first known example in Coleoptera, and several remarkable morphological modifications demonstrate an ontogenetic transformation series from female to males of different species. We discuss possible scenarios for the evolution of neoteny, precocity and fighting characteristics in these male beetles, in the light of W. D. Hamilton’s ‘ideal biofacies’ of extreme inbreeding. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 75, 353‐360. ADDITIONAL KEYWORDS: 12S ‐ CO1 ‐ Coleoptera ‐ Curculionidae ‐ EF-1a ‐ haplodiploidy ‐ ideal biofacies ‐ inbreeding ‐ molecular phylogeny ‐ Scolytinae.

Evolutionary radiation of an inbreeding haplodiploid beetle lineage (Curculionidae, Scolytinae)

Haplodiploidy is a highly unusual genetic system that has arisen at least 17 times in animals of varying lifestyles, but most of these haplodiploid lineages remain relatively poorly known. In particular, the ecological and genetic circumstances under which haplodiploidy originates have been difficult to resolve. A recent molecular-phylogenetic study has resolved the phylogenetic position of the haplodiploid clade of scolytine beetles as the sister group of the genus Dryocoetes. Haplodiploid bark beetles are remarkable in that the entire clade of over 1300 species are apparently extreme (sib-mating) inbreeders, most of which cultivate fungi for food while some attack phloem, twigs or seeds. Here we present a much more detailed molecular-phylogenetic study of this clade. Using partial sequences of elongation factor 1-alpha and the mitochondrial small ribosomal subunit (12S), we reconstructed the phylogeny for 48 taxa within the haplodiploid clade, as well as two species of the diplodiploid sister genus Dryocoetes. Results indicate that the genus Ozopemon is the basal lineage of the haplodiploid clade. Since Ozopemon, Dryocoetes, and other outgroups are phloem-feeding, this strongly suggest that haplodiploidy and inbreeding evolved in a phloem feeding ancestor. Following the divergence of Ozopemon there is a series of extremely short internodes near the base of the clade, suggesting a very rapid rate of diversification in early Miocene (based on fossil evidence and sequence divergence). Among the many substrates for breeding and food resources utilized within this species-rich clade, the cultivation of yeast-like ambrosia fungi in tunnels deep into the wood predominates (nearly 90% of the species). The number of transitions to feeding on such fungi was few, possibly only one, and is perhaps an irreversible transition. The habit of feeding on fungi cultured in xylem makes it possible for the beetles to use a great variety of plant taxa. This extreme resource generalism, in conjunction with the colonization advantage conferred by haplodiploidy and inbreeding, may have promoted the rapid diversification of this clade.

Evolutionary radiation of an inbreeding haplodiploid beetle lineage (Curculionidae, Scolytinae)

Haplodiploidy is a highly unusual genetic system that has arisen at least 17 times in animals of varying lifestyles, but most of these haplodiploid lineages remain relatively poorly known. In particular, the ecological and genetic circumstances under which haplodiploidy originates have been difficult to resolve. A recent molecular-phylogenetic study has resolved the phylogenetic position of the haplodiploid clade of scolytine beetles as the sister group of the genusDryocoetes . Haplodiploid bark beetles are remarkable in that the entire clade of over 1300 species are apparently extreme (sib-mating) inbreeders, most of which cultivate fungi for food while some attack phloem, twigs or seeds. Here we present a much more detailed molecular-phylogenetic study of this clade. Using partial sequences of elongation factor 1-alpha and the mitochondrial small ribosomal subunit (12S), we reconstructed the phylogeny for 48 taxa within the haplodiploid clade, as well as two species of the diplodiploid sister genus Dryocoetes. Results indicate that the genus Ozopemon is the basal lineage of the haplodiploid clade. Since Ozopemon, Dryocoetes, and other outgroups are phloem-feeding, this strongly suggest that haplodiploidy and inbreeding evolved in a phloem feeding ancestor. Following the divergence ofOzopemon there is a series of extremely short internodes near the base of the clade, suggesting a very rapid rate of diversification in early Miocene (based on fossil evidence and sequence divergence). Among the many substrates for breeding and food resources utilized within this species-rich clade, the cultivation of yeast-like ambrosia fungi in tunnels deep into the wood predominates (nearly 90% of the species). The number of transitions to feeding on such fungi was few, possibly only one, and is perhaps an irreversible transition. The habit of feeding on fungi cultured in xylem makes it possible for the beetles to use a great variety of plant taxa. This extreme resource generalism, in conjunction with the colonization advantage conferred by haplodiploidy and inbreeding, may have promoted the rapid diversification of this clade.

Dispersal and new colony formation in wild naked mole-rats: evidence against inbreeding as the system of mating

Early field work on naked mole-rats, Heterocephalus glaber, suggested that small colonies are rare and that colonies can only form by fissioning of existing colonies. Many researchers expected that this would result in extreme inbreeding and high relatedness within colonies and would thus explain the evolution of eusociality in naked mole-rats. Here I report evidence of dispersers and outbreeding in colonies of wild naked mole-rats that suggests that inbreeding is not the system of mating for this species and that outbreeding is probably frequent. Wild dispersers have the same morphology as was reported for dispersers in laboratory colonies. Low levels of genetic variation in previous molecular genetic studies of naked mole-rats probably result from the viscous population structure typical of fossorial rodents.

Lack of nucleotide variability in a beetle pest with extreme inbreeding.

The coffee berry borer beetle Hypothenemus hampei (Ferrari) (Curculionidae: Scolytinae) is the major insect pest of coffee and has spread to most of the coffee-growing countries of the world. This beetle also displays an unusual life cycle, with regular sibling mating. This regular inbreeding and the population bottlenecks occurring on colonization of new regions should lead to low levels of genetic diversity. We were therefore interested in determining the level of nucleotide variation in nuclear and mitochondrial genomes of this beetle worldwide. Here we show that two nuclear loci (Resistance to dieldrin and ITS2) are completely invariant, whereas some variability is maintained at a mitochondrial locus (COI), probably corresponding to a higher mutation rate in the mitochondrial genome. Phylogenetic analysis of the mitochondrial data shows only two clades of beetle haplotypes outside of Kenya, the proposed origin of the species. These data confirm that inbreeding greatly reduces nucleotide variation and suggest the recent global spread of only two inbreeding lines of this bark beetle.

EVOLUTION OF THE MAGNITUDE AND TIMING OF INBREEDING DEPRESSION IN PLANTS.

Estimates of inbreeding depression obtained from the literature were used to evaluate the association between inbreeding depression and the degree of self-fertilization in natural plant populations. Theoretical models predict that the magnitude of inbreeding depression will decrease with inbreeding as deleterious recessive alleles are expressed and purged through selection. If selection acts differentially among life history stages and deleterious effects are uncorrelated among stages, then the timing of inbreeding depression may also evolve with inbreeding. Estimates of cumulative inbreeding depression and stage-specific inbreeding depression (four stages: seed production of parent, germination, juvenile survival, and growth/reproduction) were compiled for 79 populations (using means of replicates, N = 62) comprising 54 species from 23 families of vascular plants. Where available, data on the mating system also were collected and used as a measure of inbreeding history. A significant negative correlation was found between cumulative inbreeding depression and the primary selfing rate for the combined sample of angiosperms (N = 35) and gymnosperms (N = 9); the correlation was significant for angiosperms but not gymnosperms examined separately. The average inbreeding depression in predominantly selfing species (δ = 0.23) was significantly less (43%) than that in predominantly outcrossing species (δ = 0.53). These results support the theoretical prediction that selfing reduces the magnitude of inbreeding depression. Most self-fertilizing species expressed the majority of their inbreeding depression late in the life cycle, at the stage of growth/reproduction (14 of 18 species), whereas outcrossing species expressed much of their inbreeding depression either early, at seed production (17 of 40 species), or late (19 species). For species with four life stages examined, selfing and outcrossing species differed in the magnitude of inbreeding depression at the stage of seed production (selfing δ = 0.05, N = 11; outcrossing δ = 0.32, N = 31), germination (selfing δ = 0.02, outcrossing δ = 0.12), and survival to reproduction (selfing δ = 0.04, outcrossing δ = 0.15), but not at growth and reproduction (selfing δ = 0.21, outcrossing δ = 0.27); inbreeding depression in selfers relative to outcrossers increased from early to late life stages. These results support the hypothesis that most early acting inbreeding depression is due to recessive lethals and can be purged through inbreeding, whereas much of the late-acting inbreeding depression is due to weakly deleterious mutations and is very difficult to purge, even under extreme inbreeding.

Mating systems in the sea anemone genus Epiactis

Four morphologically similar species in the sea anemone genus Epiactis exhibit overlapping distributions on the Pacific coast of North America; E. prolifera, E. lisbethae, E. ritteri and E. fernaldi. All brood their offspring up to the juvenile stage, but each has a different combination of internal versus external brooding and hermaphroditism versus gonochory (separate sexes). Specimens were collected from sites ranging from British Columbia to southern California between December 1988 and July 1992. Mating systems were inferred from genetic comparisons of mothers and offspring histological analyses of sex expression and observations on brooding and spawning behavior. Allozyme and multilocus DNA fingerprint analyses of the gynodioecious hermaphrodite E. prolifera showed that offspring were all identical to their mothers, a result consistent with either asexual reproduction, self-fertilization or extreme biparental inbreeding. In the gonochore E. lisbethae, mothers and offspring were also electrophoretically identical, but variation in DNA fingerprints indicated cross-fertilization. Similar DNA fingerprint differences between mother and offspring in the gonochore E. ritteri implied that cross-fertilization also occurs in this species. No mother-offspring comparisons were performed on E. fernaldi, as this species was not observed brooding offspring during this study. Although incomplete, the results of this study increase our knowledge of the very unusual combination of reproductive modes in the genus Epiactis, and argue for further investigations of the evolution and genetic consequences of mating systems in these species.

DNA fingerprinting in Speke's gazelle: a test for genetic distinctness, and the correlation between relatedness and similarity

In the absence of pedigree information, the determination of genetic distinctness of populations can only be made by genetic methods. Using DNA fingerprinting on the North American captive herd of Speke's gazelle Gazella spekei, we were able to address two hypotheses. First, two new individuals were found to have come from a genetically distinct population (P = 0.008, permutation test), and represent potential new founders to be added to the population. Secondly, genetic similarity was not significantly correlated with relatedness under extreme inbreeding and very close relationship (coefficient of relationship range 0.304-0.717).

Natal Philopatry, Competition for Resources, and Inbreeding Avoidance in Townsend's Voles (Microtus Townsendii)

Individuals may leave their birthsite before reproducing or they may postpone reproduction because they are at risk of engaging in inbred matings with their close relatives or because they are exposed to severe competition for resources or for mates. I studied whether avoidance of inbreeding and intrasexual competition determine the seasonal changes in the rate of philopatry and the fate of individual Townsend's voles (Microtus townsendii). By marking most nestlings before weaning, I knew which recruits were related to one another and to which adult female. There was a pronounced sexual bias in the tendency to remain close to the birth site: 9% of all juvenile males 33% of all juvenile females entered the breeding population on their natal grid. Males settled farther from their birth site than females did. The proportion of males and females reproducing on their natal grid changed markedly over the breeding season. More males and females reproduced if they were born at the beginning of the breeding season or when breeding activity was depressed by botfly infestation. Seasonal changes in female philopatry were consistent with the hypothesis that females disperse in response to competition for resources with breeding females. Females born at high adult female density were less likely to be recruited than those born at other times. They also dispersed farther at low than at high density, probably in response to habitat saturation. Avoidance of extreme inbreeding influenced the dispersal tendency of maturing males. Males were less likely to join the breeding population if their mother or a littermate sister was present in their home range when they matured than if they had no female close relatives in their home range. Males with their mother alive at sexual maturation settled farther than males whose mother had disappeared by that time. I concluded that inbreeding avoidance influenced natal philopatry in males and that competition for resources influenced natal philopatry in females.